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Surgical Resection Margin Classifications for High Modern Pathology (2019) 32:1421–1433 https://doi.org/10.1038/s41379-019-0278-9 ARTICLE Surgical resection margin classifications for high-grade pleomorphic soft tissue sarcomas of the extremity or trunk: definitions of adequate resection margins and recommendations for sampling margins from primary resection specimens 1 2 Margaret M. Cates ● Justin M. M. Cates Received: 4 February 2019 / Revised: 29 March 2019 / Accepted: 30 March 2019 / Published online: 3 May 2019 © United States & Canadian Academy of Pathology 2019 Abstract Adequacy of surgical resection margins for soft tissue sarcomas are poorly defined because of the various classifications and definitions used in prior studies of heterogeneous patient cohorts and inconsistent margin sampling protocols. Surgical resection margins of 166 primary, high-grade, pleomorphic sarcomas of the extremity or trunk were classified according to American Joint Committee on Cancer R and Musculoskeletal Tumor Society categories, as well as by metric distance and tissue composition. None of the cases were treated with neoadjuvant therapy. Multivariable competing risk regression 1234567890();,: 1234567890();,: models were evaluated and optimal surgical resection margins for each classification system were defined. Minimum safe tumor clearance was 5 mm without use of adjuvant radiotherapy and 1 mm with adjuvant radiotherapy. Predictive accuracy of margin classification systems was compared by area under receiver-operating characteristic curves generated from logistic regression of 2½-year local recurrence-free survival and other standard tests of diagnostic accuracy. The Musculoskeletal Tumor Society and margin distance classifications performed similarly, both of which showed higher sensitivity and negative predictive value compared to the American Joint Committee on Cancer R classification. The prognostic power of close or positive margins in prediction models significantly increased when six or more slides were submitted for assessment of surgical resection margins. Surgical resection margins for soft tissue sarcoma should be reported using the Musculoskeletal Tumor Society classification or metric distance to the closest resection margin. Musculoskeletal Tumor Society wide/radical margins or tumor clearances of 5 mm (without adjuvant radiotherapy) or 1 mm (with adjuvant radiotherapy) appear to define the minimum safe surgical resection margins necessary to decrease the likelihood of local recurrence of high-grade pleomorphic sarcomas of the extremity or trunk. Introduction tissue around the tumor [1]. The National Comprehensive Cancer Network continues to recommend adjuvant radio- The European Society for Medical Oncology recommends therapy for patients with soft tissue sarcoma resected with that soft tissue sarcomas of the extremity and trunk be close soft tissue (<1 cm from tumor) or positive resection excised with negative margins that include a rim of normal margins [2]. However, these recommendations are based on a limited number of studies of heterogeneous patient cohorts, particularly in regard to administration of adjuvant radiation therapy. Thus, the minimum margin distance Supplementary information The online version of this article (https:// doi.org/10.1038/s41379-019-0278-9) contains supplementary necessary to reduce the risk of local recurrence of high- material, which is available to authorized users. grade soft tissue sarcoma remains undefined. A major problem encountered when attempting to syn- * Justin M. M. Cates thesize the prior literature is the various classification [email protected] schemes used to report surgical resection margins for soft 1 Lancaster Christian Academy, Smyrna, TN 37167, USA tissue sarcoma (Table 1). The Enneking classification (since 2 Department of Pathology, Microbiology, and Immunology, adopted by the Musculoskeletal Tumor Society) has been a Vanderbilt University Medical Center, Nashville, TN 37232, USA clinically useful surgical definition of resection margin 1422 M. M. Cates, J. M. M. Cates Table 1 Classification schemes used to report surgical resection margins for soft tissue sarcoma Margin Definitions classification scheme AJCC R system R0 Grossly and microscopically negative R1 Microscopically positive R2 Grossly positive MSTS system Radical All normal tissue of involved anatomic compartments excised en bloc Wide Histologically non-reactive normal tissue at margin Marginal Pseudocapsule present at margin Fig. 1 Photomicrograph of the surgical resection margin of a high- grade pleomorphic sarcoma denoting Musculoskeletal Tumor Society Intralesional Tumor present at margin margin classifications (H&E, 40×) Margin distance Metric distance from edge of tumor to inked surgical resection margin AJCC American Joint Committee on Cancer, MSTS Musculoskeletal resected at our institution between 1995 and 2014 without Tumor Society prior neoadjuvant radiotherapy or chemotherapy. High- grade myxofibrosarcomas were excluded because this sar- coma subtype is associated with higher rates of local status since 1980 [3]. The College of American Pathologists recurrence than other sarcomas, most likely because of the instead mandates provision of a metric distance for report- tendency of the low-grade myxoid component to grow ing negative margins [4]. And the American Joint Com- along fibrous septa in subcutaneous tissues [7, 8]. Tumors mittee on Cancer R system simply reports margins as with a myxoid component were classified as undiffer- negative, microscopically positive, or grossly positive [5]. entiated pleomorphic sarcoma if <10% of the total exam- Which method of reporting status of surgical resection ined area was composed of hypocellular myxoid zones; margins is most accurate in predicting local recurrence has otherwise, the case was classified as a high-grade myxofi- not been directly analyzed. brosarcoma and excluded from the study. Dedifferentiated There is also a lack of evidence regarding the gross and liposarcomas were similarly excluded given the inherent histopathological assessment of the adequacy of surgical difficulty in differentially classifying resection margins resection margins, with one recent consensus practice involved by low-grade and high-grade sarcomatous com- guideline noting that “no available evidence-based data ponents and the better overall prognosis of these tumors [9]. addressed how to adequately assess margins” [6]. There- Resection specimens were prosected according to stan- fore, this study was performed to (1) determine the mini- dard technique [4]. Briefly, the widths of all surgical mum surgical resection margin distance necessary to reduce resection margins were evaluated grossly and metric dis- the risk of local recurrence in high-grade pleomorphic soft tances recorded; in addition to one representative section of tissue sarcomas treated with or without adjuvant radiation tumor per centimeter of its greatest dimension, all surgical therapy, (2) directly compare various margin classification resection margins ≤2 cm from tumor were inked and sam- schemes used in the literature, and (3) determine the number pled with one or more perpendicular sections. H&E-stained of tissue sections needed to adequately evaluate the status of slides were reviewed to confirm the histologic diagnosis and surgical resection margins by histopathologic examination. record the status of surgical resection margins according to American Joint Committee on Cancer and Musculoskeletal Tumor Society criteria [3, 5], as well as the margin distance Patients and methods and the tissue type composing the closest margin (pseudo- capsule, fibroadipose, skeletal muscle, or dense regular Patient cohort connective tissue [fascia or periosteum]) (Fig. 1). Clinicopathologic data, including patient age, sex, tumor The study protocol was approved by the Institutional size, adjuvant therapy administered, and clinical outcomes Review Board at Vanderbilt University; a waiver of (local recurrence-free and disease-free survival) were informed consent was obtained. Surgical Pathology files abstracted from an institutional cancer registry and cross- were searched for primary, non-cutaneous, high-grade, referenced with electronic medical records. The primary pleomorphic soft tissue sarcomas of the extremities or trunk outcome measure was local recurrence. Median follow-up Surgical resection margin classifications for high-grade pleomorphic soft tissue sarcomas of the. 1423 for censored patients was 49 months (range, Table 2 Clinicopathologic characteristics of patient cohort (N = 166) 0.7–181 months). Recurrent disease (or death from sar- Variable N (%) coma) occurred in 77 patients (46%) a median of 8 months after surgical resection (range, 0.5–62 months). Local Sex recurrence developed in 22 patients (13%) a median of Female 72 (43) 14 months after surgical resection (range, 3–49 months). Male 94 (57) Histologic diagnosis Statistical analysis Undifferentiated pleomorphic sarcoma 126 (76) Leiomyosarcoma 24 (14) Associations and correlations between variables were Pleomorphic liposarcoma 14 (8) evaluated using standard bivariate methods. Subhazard Pleomorphic rhabdomyosarcoma 2 (1) ratios for local recurrence-free and disease-free survival Anatomic depth were estimated using competing risk regression. Multi- Deep soft tissue 136 (82) variate regression models were developed through stepwise Subcutaneous tissue 30 (18) elimination of variables in order of increasing z-score. Metastasis Tumor size and adjuvant radiation therapy were retained as None 147 (89) important covariates
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